Production of Hydroxylated Polybrominated Diphenyl Ethers (OH

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Production of Hydroxylated Polybrominated Diphenyl Ethers (OH-PBDEs) from Bromophenols by Manganese Dioxide Kunde Lin,*,† Chao Yan,† and Jay Gan‡ †

College of Biological and Environmental Engineering, Zhejiang University of Technology, Hangzhou 310032, People’s Republic of China ‡ Department of Environmental Sciences, University of California, Riverside, California 92521, United States S Supporting Information *

ABSTRACT: Hydroxylated polybrominated diphenyl ethers (OH-PBDEs) are of significant concern because of their enhanced toxicological effects compared to PBDEs. Research to date has attributed the origin of OH-PBDEs to biological metabolism of PBDEs and natural production in the environment. However, it is unclear how OH-PBDEs are formed naturally. In this study, we explored the formation of OHPBDEs via the oxidative transformation of simple bromophenols (BPs, e.g., 4-BP, 2,4-DBP, and 2,4,6-TBP) by birnessite (δ-MnO2). Results showed that OH-PBDEs were readily produced by δ-MnO2 with BPs as precursors. For example, oxidation of 2,4-DBP by δ-MnO2 yielded 2′-OH-BDE-68 and 2′,5′-OH-BDE-25. Other OH-PBDEs, such as 6-OH-BDE-13, 2′,5′-OH-BDE-3, 4′-OH-BDE-121, and 2′,5′-OH-BDE-69, were detected from the reaction with 4-BP and 2,4,6-TBP. The formation of OH-PBDEs likely resulted from the oxidative coupling of bromophenoxy radicals. Mild acidic conditions enhanced while coexisting cations (e.g., Na+, Mg2+, and Ca2+) suppressed the transformation. Given the ubiquity of BPs and δ-MnO2, oxidation of BPs by δ-MnO2 and other metal oxides is likely an abiotic route for the formation of OH-PBDEs in the environment.

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INTRODUCTION Polybrominated diphenyl ethers (PBDEs) are a class of brominated flame retardants (BFRs) used extensively in textiles, construction materials, electronic equipment, and a variety of other plastic products.1 Over the past decade, PBDEs have emerged as persistent organic pollutants of great concern because of their persistence, high bioaccumulation potential, and toxicity.2 A relatively recent discovery is the prevalent occurrence of hydroxylated (OH-) and methoxylated (MeO-) PBDEs in waters,3 sediments,4 wildlife,5−8 and humans.9−11 In comparison to PBDEs, OH-PBDEs have altered or enhanced toxicological effects, such as disruption to thyroid hormone homeostasis, disruption to sex hormone steroidogenesis, and neurotoxicity.12−14 In addition, both laboratory and field studies showed that OH-PBDEs could be maternally transferred to the offspring in wildlife and humans,8−10 suggesting potential risks in multiple generations. Unlike PBDEs, OH- or MeO-PBDEs are not originally manmade chemicals. Research to date has attributed the origin of OH-PBDEs to metabolism of PBDEs and natural production in the environment.3,15−17 For example, Ueno et al. suggested that atmospheric oxidation of PBDEs may be a source of OH-PBDEs.3 Many other studies have shown that PBDEs are biologically transformed to OH-PBDEs in organisms via hydroxylation.15−17 Such metabolic processes, however, do not fully © 2013 American Chemical Society

explain the detection of OH-PBDEs in some other biota samples and environmental compartments. For example, Malmvarn et al.7 found that red algae Ceraminum tenuicorne and blue mussels from the Baltic Sea had relatively high concentrations of OHPBDEs compared to PBDEs. The researchers also identified 6-OH-BDE-137 but not the corresponding PBDE precursors in the same samples.7 Similar distribution patterns of OH-PBDEs also occurred in the blood of Baltic salmon.6,18 These observations implied natural sources of OH-PBDEs. When the natural radiocarbon abundance was analyzed, two of the most abundant congers 2′-MeO-BDE-47 and 2′-MeO-BDE-68 were determined to be naturally produced, possibly from their OHcounterparts.5 Similarly, many ortho-substituted OH-PBDEs were found to be natural products of marine algae or associated microorganisms.7,18 However, at present, it is unclear how OHPBDEs are formed in the environment. Under simulated sunlight irradiation, aqueous 2,4-dibromophenol was rapidly converted to 2′-OH-BDE-68, likely because of the formation of the 2,4-dibromophenoxy radical and its reactions with the substrate.19 A well-known pathway for the Received: Revised: Accepted: Published: 263

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production of phenoxy radicals in the environment is the oxidation of phenolic compounds by birnessite (δ-MnO2).20−22 The birnessite group of hydrous manganese oxides, with an empirical formula of [Na, Ca, MnII] Mn7O14·2.8H2O, is among the most important naturally occurring reactants or catalysts in soils and sediments.23 On the other hand, simple bromophenols [BPs, e.g., 4-bromophenol (4-BP), 2,4-dibromophenol (2,4-DBP), and 2,4,6-bromophenol (2,4,6-TBP)] are ubiquitously present in the aquatic environment because of the release from various industrial processes/products and natural biosynthesis by aquatic organisms.24 For example, reported concentrations of 2,4-DBP and 2,4,6-TBP in surface fresh water were 40 and 0.3 μg/L, respectively,24 while 2,4,6-TBP levels in surface sediment from the Rhone estuary, France, were 26−3690 μg/kg.24 However, the reaction of δ-MnO2 with BPs has yet to be characterized, and it is unknown if OH-PBDEs may be derived from BPs. The objective of this study was to evaluate the oxidative transformation of BPs to OH-PBDEs by synthetic δ-MnO2. Specifically, we tested the possibility of the formation of OHPBDEs and explored the pathways. The effects of δ-MnO2 loading, pH, and coexisting metal ions on the conversion were also examined.

during reaction. Briefly, aliquots of 5 mL of reaction mixture were periodically withdrawn and passed through Millex 0.22 μm polyvinylidene fluoride membrane filters (Millipore, Billerica, MA). The filtrates were acidified with 3 drops of concentrated nitric acid and analyzed for Mn2+ concentrations by atomic absorption spectroscopy. To evaluate the effect of pH, reactions were maintained under pH 4.50, 6.50, 7.50, and 8.50 (with a range of variation of ±0.15 pH) by manually adding 0.1 M HCl or NaOH into the reaction solutions. No buffers were used in this study to exclude the possible interference of buffer components. A previous test showed that the small change of ion strength resulting from the addition of HCl or NaOH had negligible effects on the reaction. In the pH 4.50 solutions, pH remained at 4.50 ± 0.10 without the addition of HCl or NaOH. Other reactions were carried out in pH 4.50 solutions unless otherwise specified. To evaluate the effect of water salinity on the conversion, various concentrations of NaCl, MgCl2, or CaCl2 were added to the solutions and the transformation of BPs was evaluated. Briefly, solutions were separately fortified with certain amounts of NaCl, MgCl2, and CaCl2, and then the reactions were initiated by adding BPs and δ-MnO2 to the solutions, as described above. Chemical Analysis. For reaction product identification, 2 mg/L 4-BP, 2,4-DBP, or 2,4,6-TBP was separately reacted with 100 μM δ-MnO2 in 100 mL of pH 4.5 solutions and the reaction was quenched after 1, 2, 4, 6, 8, 12, and 16 h by adding 0.5 mL of 5 mg/mL ascorbic acid. The quenched solution was extracted with 6 mL Oasis hydrophilic−lipophilic balance (HLB) solid-phase extraction (SPE) cartridges (Waters, Millford, MA). Prior to extraction, each SPE cartridge was sequentially preconditioned with 5 mL of methanol and 5 mL of reagent water. The reaction solution was then loaded onto the SPE cartridge at a flow rate of 3 mL/min using a Supelco vacuum manifold (Bellefonte, PA), and then the cartridge was rinsed with 5 mL of ultrapure water and dried under a stream of nitrogen for 30 min. The cartridge was eluted with 10 mL of methanol, and the eluent was condensed to dryness on a vacuum rotary evaporator. The extract was finally redissolved in 100 μL of acetone/hexane (50:50, v/v). The final samples were analyzed on an Agilent 7890A gas chromatograph (GC) coupled with an Agilent model 5975C mass spectrometer (MS) (Agilent Technologies, Wilmington, DE) for chemical structural elucidation. A HP5MS column (30 m × 0.25 mm × 0.25 μm, Agilent) was used for separation. The inlet temperature was 300 °C. The oven temperature was initiated at 60 °C, increased to 300 °C at 10 °C/min, and held for 20 min. The flow rate of the carrier gas (helium) was 1.0 mL/min. The injection of a 2 μL sample was carried out by an Agilent model 7693 autosampler in a pulsed splitless mode turning on after 1.0 min. The temperatures of the transfer line, ion source, and MS detector were 300, 230, and 150 °C, respectively. The MS detector was operated in an electron impact mode at 70 eV, and the mass spectra were acquired in a full-scan mode with m/z ranging from 50 to 600 amu. To further verify the chemical structures of reaction products, samples were methylated.26 Briefly, the final extracts were redissolved in 3 mL of acetone, followed by the addition of iodomethane (120 μL) and tetrabutylammonium hydroxide (60 μL). The sample vials were immediately sealed, vortexed, and incubated in a 40 °C water bath for 1.5 h. Each sample volume was then reduced to approximately 1 mL under a gentle flow of nitrogen. Samples were brought up to 4 mL with hexane and mixed with sulfuric acid (2.0 mL, 0.5 M). The organic layer

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MATERIALS AND METHODS Chemicals. Standards of 4-BP (>99%), 2,4-DBP (>95%), and 2,4,6-TBP (>98%) and methylation reagents iodomethane (99.5%) and tetrabutylammonium hydroxide solution (40% in water) were purchased from Sigma-Aldrich (St. Louis, MO). Authentic standards of 2′-hydroxy-2,3′,4,5′-tetraBDE (2′-HOBDE-68) were purchased from AccuStandard (New Haven, CT). Reagent water (18.2 MΩ cm resistivity) was prepared using a Millipore water purification system (Millipore S.A.S., Molsheim, France). Other chemicals were of analytical or highperformance liquid chromatography (HPLC) grade. Manganese dioxide (δ-MnO2) was synthesized according to Murray’s method.25 Briefly, 2.46 L of deionized water was purged with nitrogen gas (N2) for 2 h prior to use, and 120 mL of 0.1 M KMnO4 and 240 mL of 0.1 M NaOH solutions were added, followed by a dropwise addition of 180 mL of 0.1 M MnCl2 while keeping the solution constantly sparged with N2. The formed δ-MnO2 particles were collected by centrifugation and rinsed with deionized water several times until the conductivity of the supernatant was less than 2 μS/cm. The resulting δ-MnO2 suspensions were stored at 4 °C and diluted to appropriate concentrations prior to use. A portion of the synthetic δ-MnO2 was freeze-dried, and its surface area was determined to be 388 m2/g by the Brunauer−Emmett−Teller (BET) method of N2 adsorption (Micromeritics ASAP 2020, Norcross, GA). Reaction Setup. All glassware was soaked in a 1 g/L ascorbic acid solution for several hours and thoroughly rinsed with deionized water prior to use. Experiments were conducted in 250 mL glass Erlenmeyer flasks at 25 ± 1 °C. Reaction mixtures (100 mL) were constantly stirred with Teflon-coated magnetic stir bars at 180 rpm. Reactions were initiated by adding 40 μL of 5 g/L BP solution to δ-MnO2 suspensions. Aliquots of 1 mL of reaction mixture were periodically collected in 1.5 mL HPLC vials containing 5 μL of 50 mg/mL ascorbic acid solution. The remaining δ-MnO2 in the sample was immediately dissolved by ascorbic acid, and the adsorbed BP was released. The resulting samples were subjected to HPLC analysis to determine the residual concentration of BPs. Meanwhile, a set of treatments were included to investigate the release of MnII 264

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those that are less reactive.29,30 In such cases, the continuous change of δ-MnO2 reactivity can be represented by a timedependent rate constant31

was collected, and the sulfuric acid phase was extracted 2 more times with 3 mL of hexane. The organic phase was combined, concentrated, and reconstituted in 100 μL of acetone/hexane (50:50, v/v). The methylated samples were analyzed on a Varian 3800 GC (Varian Instruments, Sunnyvale, CA) coupled with a Varian 1200 triple-quadrupole mass spectrometer (MS/ MS). Separation was achieved on an Agilent DB-5MS capillary column (60 m × 0.25 mm × 0.25 μm). A 2.0 μL aliquot of the final methylated sample was injected at 250 °C in the splitless mode at a constant flow of 1 mL/min. Helium (99.999%) was used as the carrier gas. The oven temperature was programmed to start at 80 °C, hold for 3 min, then increase at 20 °C/min to 300 °C, and be kept for 15 min. The MS/MS electron ionization source was 70 eV, and the transfer line, manifold, and ionization source temperatures were 300, 40, and 170 °C, respectively. Argon (99.9999%) was used as the collision gas, with a resolution of quadrupoles of 1.0 for both Q1 and Q3. The analytical procedures for the residual concentrations of BPs and MnII in the collected samples are given in Text S1 of the Supporting Information.

kt =

k init 1 + αt

(1)

−1

where kt (min ) is the reaction rate constant at time t, kinit is the initial apparent reaction rate constant, and α (min−1) is a retarded factor describing the decrease of kt over time. When α equals 0 (a first-order reaction), kt is a constant and equals kinit. Apparently, a higher value of α suggests a faster decrease of kt with time. Accordingly, the retarded first-order rate equation can be expressed as31 −

dCt k init = Ct dt 1 + αt

(2)

Integration of eq 2 yields the retarded first-order rate equation Ct = C0(1 + αt )−k init / α

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(3)

where Ct (μM) is the concentration of BPs at time t and C0 (μM) is the initial concentration of BPs. All reactions of BPs with δ-MnO2 in this study were welldescribed by eq 3, with model fit R2 values ranging from 0.96 to 0.99 (see Tables S1 and S2 of the Supporting Information). Various values of retarded factor α (α ≠ 0) were obtained for the different treatments. The good fit of the reactions to eq 3 suggested that the time-dependent kt was a suitable indicator to represent the decline of rate constants. Identification of OH-PBDEs. The intermediates and products formed from the reaction of BPs (4-BP, 2,4-DBP, and 2,4,6-TBP) with δ-MnO2 were identified by GC−MS and GC−MS/MS. The retention times, mass spectra, and assignments of major fragment ions for the identified compounds are presented in Figures 2 and 3 and Figures S1−S9 of the Supporting Information. Six of the compounds were tentatively identified as OH-PBDEs (Figure 4). For example, in the reaction of eq 2, 4-DBP with δ-MnO2, all mass spectra of the products show strong evidence of the presence of bromine atom(s). Each of the precursor ions has the stable isotope peaks 79Br (50.69%) and 81Br (49.31%), and the fragment ions apparently include m/z M − 80 (M−Br) and/or M − 160 (M−Br2), with M referring the precursor ion of an identified compound (Figures 2 and 3 and Figures S1−S9 of the Supporting Information). The non-methylated compounds eluted at 23.469 and 23.582 min both had precursor ions of m/z 502, suggesting that they were structural isomers. The second eluted constituent was verified to be 2′-OH-BDE-68, with a good match in retention time and mass spectra with the authentic standard (see Figure S1 of the Supporting Information). The possible assignments for the major fragment ions of m/z 502, 422, 342, 262, 236, and 171 are given in Figure 2. In addition to the major fragment ions present in 2′-OH-BDE-68, the first eluted constituent showed a strong base peak of m/z 484 (M − H2O) (Figure 3), indicating the loss of H2O during GC−MS analysis. A possible isomer is 2,2′dihydroxy-3,3′,5,5′-tetrabrominated biphenyl (2,2′-OH-BB-80). In addition, 2′,5′-dihydroxy-2,3′,4-triBDE (2′,5′-OH-BDE-25) was tentatively identified to be a reaction product (see Figure S3 of the Supporting Information). The constituent at 10.810 min was identified to be 2-bromohydroquinone from the search in the National Institute of Standards and Technology (NIST) mass spectral library (see Figure S2 of the Supporting Information). To further verify that the detected OH-PBDEs

RESULTS AND DISCUSSION Transformation Kinetics. All of the selected BPs were rapidly transformed by δ-MnO2 in the reaction solutions (Figure 1). For example, consumptions of 4-BP, 2,4-DBP, and

Figure 1. Transformation of BPs by 100 μM δ-MnO2 in pH 4.5 solutions at 25 ± 1 °C. Lines are the residual BP fit to the retarded first-order rate equation (eq 3). Dash lines are the evolution of Mn2+ over reaction time. The initial concentrations of 4-BP, 2,4-DBP, and 2,4,6-TBP were all 7.94 μM. Error bars are standard deviations of triplicate measurements.

2,4,6-TBP by 100 μM δ-MnO2 in 100 min were approximately 71, 94, and 99%, respectively. Transformation of BPs was apparently accompanied by the liberation of MnII, suggesting the concurrent reduction of MnIV to MnII. However, a stoichiometric calculation for the reduction of MnIV could not be made because of the strong adsorption of MnII by δ-MnO2.27,28 The increasing concentrations of freely dissolved MnII over time suggested the continuous reaction of δ-MnO2 with the substrates (or intermediates) under the experimental conditions. In general, changes in the concentration of BPs could not be described by the first-order decay model because of the apparent decreasing rate constant as the reaction proceeded. This phenomenon is commonly observed in the reaction of δ-MnO2 with organic compounds,29,30 likely because of the surface alteration resulting from the adsorption of reaction products and shifts in the distribution of surface sites toward 265

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Figure 2. Mass spectra and the interpretation of detected 2′-OH-BDE-68 and its methylated derivative.

intermediates analogous to 2′-OH-BDE-68. Semi-quantitative analysis of the other detected OH-PBDEs and 2,2′-OH-BB-80 was carried out on the basis of peak area in the chromatogram of GC−MS analysis. The evolution profiles are given in Figure 5. Overall, some of the OH-PDBEs (e.g., 6-OH-BDE-13 and 2′-OH-BDE-28) increased steadily over time, while the others (e.g., 2′,5′-OH-BDE-3 and 2′,5′-OH-BDE-25) increased in the first few hours and then decreased thereafter. The decrease of these OH-PBDEs suggested that they underwent further oxidation. Formation Pathways. The oxidation of phenolic compounds by δ-MnO2 generally involves several major processes, i.e., (i) formation of a precursor complex between the organic compound and the oxide surface, (ii) electron transfer from the organic compound to the oxide, (iii) release of the phenoxy radical and reduced MnII, and (iv) radical coupling and other further reactions.20−22 On the basis of the general reaction mechanism and detected intermediates, possible pathways for the formation of OH-PBDEs are presented in Figure 4. In the proposed scheme, oxidation of BPs is initiated by transferring electrons to δ-MnO2, yielding bromophenoxy radicals. The unpaired electron in the bromophenoxy radical is likely to delocalize to new positions, forming other transition radicals (pathway I). The radicals thereafter may undergo coupling reactions and further oxidation by δ-MnO2. Generally, the coupling processes involve carbon−carbon (C−C) and carbon−oxygen (C−O) combination of the mesomeric radicals.32 In the reaction of eq 2, 4-DPB with δ-MnO2, for example, para C−O coupling followed by enolization generates

were not structural isomers of dihydroxylated polybrominated biphenyls (di-OH-PBB), all of the samples were methylated to replace −OH group(s) with −OCH3. Therefore, a methylated derivative of a di-OH-PBB has one more −OH replacement than its OH-PBDE isomer, showing a molecular weight increase by 14 (−CH2). For example, the molecular weights of methylated 2′-OH-BDE-68 and 2,2′-OH-BB-80 are 516 and 530, respectively (Figures 2 and 3). All full scans and MS/MS analyses of the methylated products (Figures 2 and 3 and Figures S1 and S3 of the Supporting Information) coincided well with the identified OH-PBDEs. Similarly, major products for the reaction of 4-BP with δ-MnO2 were identified to be hydroquinone, 6-hydroxy-3,4′-diBDE (6-OH-BDE-13), and 2′,5′-dihydroxy-4-monoBDE (2′,5′-OHBDE-3), while 2,6-dibromohydroquinone, 4′-hydroxy2,3′,4,5′,6-pentaBDE (4′-OH-BDE-121), and 2′,5′-dihydroxy2,3′,4,6-tetraBDE (2′,5′-OH-BDE-69) were found to be the reaction products of 2,4,6-TBP. Except for 2′-OH-BDE-68, authentic standards of the other possible OH-PBDEs were not available, and the identification was therefore tentative. The detailed information on the structural elucidation of these compounds is given in Figures S1−S9 of the Supporting Information. The yield of 2′-OH-BDE-68 from 2,4-DBP in 16 h under the experimental conditions was estimated to be 2.2%. The yields of the other intermediates could not be calculated because of the lack of authentic standards. Although the yield of 2′-OHBDE-68 appeared small, the total production of OH-PBDEs from the reaction may be very substantial because radical coupling reactions may result in the formation of many 266

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Figure 3. Mass spectra and the interpretation of detected 2,2′-OH-BB-80 and its methylated derivative.

2′-OH-BDE-68 (pathway II-i), while ortho−ortho C−C coupling produces 2,2′-OH-BB-80 (pathway II-ii). The 2,4-DBP radical may undergo further oxidation by δ-MnO2, yielding 2-bromohydroquinone (pathway II-iii). It can be expected that 2-bromohydroquinone is also susceptible to the oxidation by δ-MnO2, releasing new radicals.22 The further couplings of 2,4-DBP and 2-bromohydroquinone radicals via similar reaction pathways result in other OH-PBDEs, such as 2′,5′-OH-BDE-25 (pathways II-iv). Likewise, products in the reaction of δ-MnO2 with 4-BP may be explained by similar pathways (Figure 4). Reactions of 2,4,6-TBP radicals may be different because of the presence of bromine at all ortho and para positions. The presence of bromine substituents has been shown to favor the formation of C−O coupling products over C−C coupling products during the oxidation of 2,4,6-TBP by a bromoperoxidase because of the possible steric effects.33 The radical coupling of 2,4,6-TBP followed by the elimination of bromine yields 4′-OH-BDE-121 (pathway IV-i). In addition, 2′,5′-OH-BDE-69 and 2,5-dribromohydroquinone may have

formed via pathways similar to those described above (pathways IV-ii and IV-iii). Effect of δ-MnO2 Dosage, pH, and Coexisting Metal Ions. A higher concentration of δ-MnO2 facilitated the oxidation of BPs. For example, 2,4-DBP dissipation in the reaction mixture increased with increasing initial concentrations of δ-MnO2 (see Figure S10 of the Supporting Information). In addition, the increase of initial rate constants kinit was directly proportional to the concentration of δ-MnO2 (see Figure S10 of the Supporting Information). Similar results were also observed for the reaction of δ-MnO2 with 4-BP and 2,4,6-TBP (data not shown). The oxidation of organic compounds by δ-MnO2 is believed to be initiated by surface reactions on the oxide, where the reductant complexes with the oxide and subsequently loses electrons to the oxide, yielding a phenoxy radical.20−22 Accordingly, higher concentrations of δ-MnO2 provided more reactive sites and, hence, accelerated the reaction. The reaction of δ-MnO2 with BPs was strongly pH-dependent. For example, the reactivity of δ-MnO2 with 2,4-DBP significantly 267

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Figure 4. Proposed pathways for the formation of OH-PBDEs via the reaction of BPs with δ-MnO2.

kinit = −0.25pH + 0.67 (R2 = 0.99), suggesting that the reaction was an acid-driven process. The reactions of many other organic compounds with δ-MnO2 were also pH-sensitive.20,22,29,34

decreased as the pH increased from 4.50 to 8.50 (Figure 6). Both kinit and α varied with pH (see Table S3 of the Supporting Information). The overall dependence may be expressed as log 268

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adsorption of the compound onto the oxide surface because of the growing electrostatic repulsion, which consequently made the subsequent reactions less favorable. The transformation of 2,4-DBP by δ-MnO2 was consistently suppressed by coexisting metal ions, i.e., Ca2+, Mg2+, and Na+ (Figure 6 and Table S3 of the Supporting Information). The inhibitory effects varied with the species and concentration of metal ions. In general, the inhibitory capacity followed the order Ca2+ > Mg2+ > Na+, with higher concentrations exhibiting stronger suppressive effects. Previous studies also showed that transitional metal ions (e.g., Fe3+ and Mn2+) and alkaline earth metal ions (e.g., Ca2+ and Mg2+) generally inhibited the reaction of δ-MnO2 with other organic compounds.34,37,38 The interaction of cations with δ-MnO2 may be responsible for the suppressive effects. Metal ions tend to adsorb on the δ-MnO2 surface because of electrostatic attraction of cations by the negative charge on the oxide.27 Exchange sorption appeared to be the principal mechanism involved in the uptake of cations.28 The affinity of the cations to δ-MnO2 followed the order Ca2+ > Mg2+ > Na+,27 consistent with the inhibitory power observed in this study. The sorption of cations inhibited the reactivity of δ-MnO2. First, the adsorption of cations may occupy the reactive sites on the δ-MnO2 surface, blocking the access of organic compounds.25,37 On the other hand, exchange sorption with cations altered the surface structure of δ-MnO2 and destabilized the oxide.28 In this study, higher concentrations (1 and 10 mM) of Ca2+ and Mg2+ cations apparently caused coagulation− flocculation of the colloidal oxide (see Figure S11 of the Supporting Information). In contrast, this phenomenon was only observed in treatments with 10 mM Na+, suggesting a weaker ability for Na+ to destabilize the oxide. Environmental Implications. This study clearly demonstrated that BPs may undergo catalytic oxidation by δ-MnO2 to

Figure 5. Semi-quantitative analysis of the transformation products for the reaction of (A) 4-BP and (B) 2,4-DBP with 100 μM δ-MnO2 in pH 4.5 solutions at 25 ± 1 °C. The initial concentrations of 4-BP and 2,4-DBP were 7.94 μM. Peak areas were calculated on the basis of the precursor ions of each compound in GC−MS analysis.

The pH effect on the reaction may be attributed to the following factors. First, the charge on the δ-MnO2 surface is dependent upon pH. According to a reported pH point of zero charge of 2.4 for δ-MnO2,25 the oxide exhibited a net negative charge over the pH range of 4.50−8.50 and the net charge increased linearly as pH increased.29 In addition, the reduction potential of δ-MnO2 has a linear dependence upon pH [e.g., 1/2MnO2(s) + 2 H+ + e → 1/2Mn2+(aq) + H2O]. For example, the reduction potential of δ-MnO2 decreased from 0.99 to 0.76 V when pH was increased from 4.0 to 8.0.35 Furthermore, pH influenced the speciation of 2,4-DBP, which may have affected the association and electron-transfer processes between 2,4-DBP with δ-MnO2 during surface reactions. The acid dissociation constant pKa of 2,4-DBP is 7.79,36 indicating a speciation shift from protonated 2,4-DBP to the deprotonated form as the pH was increased from 4.50 to 8.50. The increase of net negative charges on the δ-MnO2 surface and species of deprotonated 2,4-DBP hindered the

Figure 6. Effect of (A) pH, (B) NaCl, (C) MgCl2, and (D) CaCl2 on the transformation of 2,4-DBP by 100 μM δ-MnO2 at 25 ± 1 °C. Lines are the residual 2,4-DBP fit to the retarded first-order rate equation (eq 3). Reactions were carried out in pH 4.5 solutions unless otherwise specified. The initial concentration of 2,4-DBP was 7.94 μM. Error bars are standard deviations of triplicate measurements. 269

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form OH-PBDEs under ambient conditions. Interestingly, 2′-OH-BDE-68, a reaction product identified in this study for the reaction of 2, 4-DBP with δ-MnO2, is one of the most naturally abundant OH-PBDE congeners.3,4,6−8 However, the other OH-PBDEs tentatively identified were not previously documented, most likely because of the lack of authentic standards for their analysis. In general, the formation of OHPBDEs may be assumed to derive from the C−O coupling of bromophenoxy radicals that are produced via the oxidation of BPs by δ-MnO2. Naturally occurring δ-MnO2 may vary greatly in different environmental compartments. For example, the average content of MnO2 was as high as 7 μM in the sediment/ water interface from Lake Zurich and up to 175 μmol/cm3 in marine sediments from the Skagerrak Sea.39,40 Acidic conditions accelerated the reaction, while coexisting metal ions (i.e., Na+, Mg2+, and Ca2+) suppressed the reaction. Usually, the concentrations of Na+, Mg2+, and Ca2+ are less than 1 mM in river waters and may be greater than 10 mM in saline lakes or seawater.35 The production of OH-PBDEs in the environment may be lower, because the concentrations of BPs and MnO2 are generally lower than those used in this study and phenoxy radicals may also react with natural organic matter. Nevertheless, given the widespread occurrence of both BPs and δ-MnO2 in aquatic environments, the transformation of BPs by manganese oxides and potentially other mineral oxides may be an abiotic route for the natural production of OH-PBDEs. The relative importance of this source should be further evaluated in the context of the global geochemical cycle of PBDEs and OHPBDEs.

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ASSOCIATED CONTENT

S Supporting Information *

Analysis of residual BPs and MnII concentrations (Text S1), retarded rate model parameters (Tables S1−S3), and mass spectra, effect of δ-MnO2 concentrations on the transformation of 2,4-DBP in pH 4.5 solution at 25 ± 1 °C, and destabilization of δ-MnO2 by Ca2+, Mg2+, and Na+ after 20 min of reaction (Figures S1−S11). This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Telephone: +86-571-88320778. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was jointly supported by the National Natural Science Foundation of China (21277124, 21320102007, and 21077091) and the Zhejiang Provincial Natural Science Foundation of China (LR13B070007).

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REFERENCES

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